Publications by authors named "Michel Paques"

121 Publications

Retinal blood flow reversal quantitatively monitored in out-of-plane vessels with laser Doppler holography.

Sci Rep 2021 09 8;11(1):17828. Epub 2021 Sep 8.

Institut Langevin. Centre National de la Recherche Scientifique (CNRS). Paris Sciences & Lettres (PSL University). École Supérieure de Physique et de Chimie Industrielles (ESPCI Paris), 1 rue Jussieu, 75005, Paris, France.

Laser Doppler holography is a planar blood flow imaging technique recently introduced in ophthalmology to image human retinal and choroidal blood flow non-invasively. Here we present a digital method based on the Doppler spectrum asymmetry that reveals the local direction of blood flow with respect to the optical axis in out-of-plane vessels. This directional information is overlaid on standard grayscale blood flow images to depict flow moving towards the camera in red and flow moving away from the camera in blue, as in ultrasound color Doppler imaging. We show that thanks to the strong contribution of backscattering to the Doppler spectrum in out-of-plane vessels, the local axial direction of blood flow can be revealed with a high temporal resolution, which enables us to evidence pathological blood flow reversals. We also demonstrate the use of optical Doppler spectrograms to quantitatively monitor retinal blood flow reversals.
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http://dx.doi.org/10.1038/s41598-021-96877-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8426375PMC
September 2021

Unsupervised Approaches for the Segmentation of Dry ARMD Lesions in Eye Fundus cSLO Images.

J Imaging 2021 Aug 11;7(8). Epub 2021 Aug 11.

Clinical Imaging Center 1423, Quinze-Vingts Hospital, INSERM-DGOS Clinical Investigation Center, 75012 Paris, France.

Age-related macular degeneration (ARMD), a major cause of sight impairment for elderly people, is still not well understood despite intensive research. Measuring the size of the lesions in the fundus is the main biomarker of the severity of the disease and as such is widely used in clinical trials yet only relies on manual segmentation. Artificial intelligence, in particular automatic image analysis based on neural networks, has a major role to play in better understanding the disease, by analyzing the intrinsic optical properties of dry ARMD lesions from patient images. In this paper, we propose a comparison of automatic segmentation methods (classical computer vision method, machine learning method and deep learning method) in an unsupervised context applied on cSLO IR images. Among the methods compared, we propose an adaptation of a fully convolutional network, called W-net, as an efficient method for the segmentation of ARMD lesions. Unlike supervised segmentation methods, our algorithm does not require annotated data which are very difficult to obtain in this application. Our method was tested on a dataset of 328 images and has shown to reach higher quality results than other compared unsupervised methods with a F1 score of 0.87, while having a more stable model, even though in some specific cases, texture/edges-based methods can produce relevant results.
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http://dx.doi.org/10.3390/jimaging7080143DOI Listing
August 2021

Laser Doppler holography of the anterior segment for blood flow imaging, eye tracking, and transparency assessment.

Biomed Opt Express 2021 Jul 28;12(7):4478-4495. Epub 2021 Jun 28.

Paris Eye Imaging, France.

Laser Doppler holography (LDH) is a full-field blood flow imaging technique able to reveal human retinal and choroidal blood flow with high temporal resolution. We here report on using LDH in the anterior segment of the eye without making changes to the instrument. Blood flow in the bulbar conjunctiva and episclera as well as in corneal neovascularization can be effectively imaged. We additionally demonstrate simultaneous holographic imaging of the anterior and posterior segments by simply adapting the numerical propagation distance to the plane of interest. We used this feature to track the movements of the retina and pupil with high temporal resolution. Finally, we show that the light backscattered by the retina can be used for retro-illumination of the anterior segment. Hence digital holography can reveal opacities caused by absorption or diffusion in the cornea and eye lens.
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http://dx.doi.org/10.1364/BOE.425272DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8367265PMC
July 2021

Normalization of series of fundus images to monitor the geographic atrophy growth in dry age-related macular degeneration.

Comput Methods Programs Biomed 2021 Sep 12;208:106234. Epub 2021 Jun 12.

Clinical Investigation Center 1423, Quinze-Vingts Hospital, 28 rue de Charenton, 75012 Paris, France.

Background And Objective: Age-related macular degeneration (ARMD) is a degenerative disease that affects the retina, and the leading cause of visual loss. In its dry form, the pathology is characterized by the progressive, centrifugal expansion of retinal lesions, called geographic atrophy (GA). In infrared eye fundus images, the GA appears as localized bright areas and its growth can be observed in series of images acquired at regular time intervals. However, illumination distortions between the images make impossible the direct comparison of intensities in order to study the GA progress. Here, we propose a new method to compensate for illumination distortion between images.

Methods: We process all images of the series so that any two images have comparable gray levels. Our approach relies on an illumination/reflectance model. We first estimate the pixel-wise illumination ratio between any two images of the series, in a recursive way; then we correct each image against all the others, based on those estimates. The algorithm is applied on a sliding temporal window to cope with large changes in reflectance. We also propose morphological processing to suppress illumination artefacts.

Results: The corrected illumination function is homogeneous in the series, enabling the direct comparison of grey-levels intensities in each pixel, and so the detection of the GA growth between any two images. To demonstrate that, we present numerous experiments performed on a dataset of 18 series (328 images), manually segmented by an ophthalmologist. First, we show that the normalization preprocessing dramatically increases the contrast of the GA growth areas. Secondly, we apply segmentation algorithms derived from Otsu's thresholding to detect automatically the GA total growth and the GA progress between consecutive images. We demonstrate qualitatively and quantitatively that these algorithms, although fully automatic, unsupervised and basic, already lead to interesting segmentation results when applied to the normalized images. Colored maps representing the GA evolution can be derived from the segmentations.

Conclusion: To our knowledge, the proposed method is the first one which corrects automatically and jointly the illumination inhomogeneity in a series of fundus images, regardless of the number of images, the size, shape and progression of lesion areas. This algorithm greatly facilitates the visual interpretation by the medical expert. It opens up the possibility of treating automatically each series as a whole (not just in pairs of images) to model the GA growth.
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http://dx.doi.org/10.1016/j.cmpb.2021.106234DOI Listing
September 2021

Adaptive optics ophthalmoscopy: a systematic review of vascular biomarkers.

Surv Ophthalmol 2021 Jun 6. Epub 2021 Jun 6.

Paris Eye Imaging Group, Centre Hospitalier National d'Ophtalmologie des Quinze-Vingts, INSERM-DHOS Clinical Investigation Center, Paris, France.

Retinal vascular diseases are a leading cause for blindness and partial sight certifications. By applying adaptive optics (AO) to conventional imaging modalities, the microstructures of the retinal vasculature can be observed with high spatial resolution, hence offering a unique opportunity for the exploration of the human microcirculation. The objective of this systematic review is to describe the current state of retinal vascular biomarkers imaged by AO flood illumination ophthalmoscopy (FIO) and AO scanning laser ophthalmoscopy (SLO). A literature research was conducted in the PubMed and Scopus databases on July 9, 2020. From 217 screened studies, 42 were eligible for this review. All studies underwent a quality check regarding their content. A meta-analysis was performed for the biomarkers reported for the same pathology in at least three studies using the same modality. The most frequently studied vascular biomarkers were the inner diameter (ID), outer diameter (OD), parietal thickness (PT), wall cross-sectional area (WCSA), and wall-to-lumen ratio (WLR). The applicability of AO vascular biomarkers has been mostly explored in systemic hypertension using AO FIO and in diabetes using AO SLO. The result of the meta-analysis for hypertensive patients showed that WLR, PT, and ID were significantly different when compared to healthy controls, while WCSA was not (P < 0.001, P = 0.002, P < 0.001, and P = 0.070, respectively). The presented review shows that, although a substantial number of retinal vascular biomarkers have been explored in AO en face imaging, further clinical research and standardization of procedures is needed to validate such biomarkers for the longitudinal monitoring of arterial hypertension and other diseases.
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http://dx.doi.org/10.1016/j.survophthal.2021.05.012DOI Listing
June 2021

Assessing Photoreceptor Status in Retinal Dystrophies: From High-Resolution Imaging to Functional Vision.

Am J Ophthalmol 2021 May 14;230:12-47. Epub 2021 May 14.

From the Department of Ophthalmology, University of Pittsburgh School of Medicine and Medical Center, Pittsburgh, Pennsylvania, USA (J.-A.S.); Sorbonne Université, Paris, France (J.-A.S.); Quinze Vingts National Ophthalmology Hospital, Paris, France (K.G., S.M.-S., M.P., I.A., A.-E.C.-R., L.A.); StreetLab - Institut de la Vision, Paris, France (C.P., C.A., K.B., E.G.); and Institut de la Vision, Paris, France (M.P., I.A., T.L., C.Z., S.P., D.D., K.M.).

Purpose: To describe the value of integrating phenotype/genotype data, disease staging, and evaluation of functional vision in patient-centered management of retinal dystrophies.

Methods: (1) Cross-sectional structure-function and retrospective longitudinal studies to assess the correlations between standard fundus autofluorescence (FAF), optical coherence tomography, visual acuity (VA), and perimetry (visual field [VF]) examinations to evaluate photoreceptor functional loss in a cohort of patients with rod-cone dystrophy (RCD); (2) flood-illumination adaptive optics (FIAO) imaging focusing on photoreceptor misalignment and orientation of outer segments; and (3) evaluation of the impact of visual impairment in daily life activities, based on functional (visual and mobility) vision assessment in a naturalistic environment in visually impaired subjects with RCD and subjects treated with Luxturna® for RPE65-related Leber congenital amaurosis before and after therapy.

Results: The results of the cross-sectional transversal study showed that (1) VA and macular sensitivity were weakly correlated with the structural variables; and (2) functional impairment (VF) was correlated with reduction of anatomical markers of photoreceptor structure and increased width of autofluorescent ring. The dimensions of the ring of increased FAF evolved faster. Other criteria that differed among groups were the lengths of the ellipsoid zone, the external limiting membrane, and the foveal thickness. FIAO revealed a variety of phenotypes: paradoxical visibility of foveal cones; heterogeneous brightness of cones; dim, inner segment-like, and RPE-like mosaic. Directional illumination by varying orientation of incident light (Stiles-Crawford effect) and the amount of side illumination (gaze-dependent imaging) affected photoreceptor visibility. Mobility assessment under different lighting conditions showed correlation with VF, VA, contrast sensitivity (CS), and dark adaptation, with different predictive values depending on mobility study paradigms and illumination level. At high illumination level (235 lux), VF was a predictor for all mobility performance models. Under low illumination (1 and 2 lux), VF was the most significant predictor of mobility performance variables, while CS best explained the number of collisions and segments. In subjects treated with Luxturna®, a very favorable impact on travel speed and reduction in the number of collisions, especially at low luminance, was observable 6 months following injection, in both children and adults.

Conclusions: Our results suggest the benefit of development and implementation of quantitative and reproducible tools to evaluate the status of photoreceptors and the impact of both visual impairment and novel therapies in real-life conditions.
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http://dx.doi.org/10.1016/j.ajo.2021.04.013DOI Listing
May 2021

[Management of toxicities of BRAF inhibitors and MEK inhibitors in advanced melanoma].

Bull Cancer 2021 May 31;108(5):528-543. Epub 2021 Mar 31.

AP-HP, hôpital Antoine-Béclère, service d'hépato-gastroentérologie et nutrition, 92140 Clamart, France; Université Paris-Saclay, inflammation, microbiome and immunosurveillance, Inserm U996, 92140 Clamart, France.

Major therapeutic advances have been made recently in the treatment of metastatic melanoma, due to the development of targeted therapies, namely BRAF and MEK inhibitors, in patients with BRAF V600 mutation. Combinations of vemurafenib+cobimetinib, dabrafenib+trametinib, et encorafenib+binimetinib, evaluated in coBRIM, COMBI-d/COMBI-v and COLUMBUS trials respectively have been approved in this indication. Toxicities induced by combination therapies are different from those reported with monotherapies, in terms of frequency and intensity. Physicians who treat melanoma patients thus face news issues relating to prevention, detection and treatment of these adverse events. This paper summarizes tolerance data from the three pivotal trials (coBRIM, COMBI-v and COLUMBUS) and issues recommendations for the specific management of main toxicities, based on experts' opinion. We discuss dermatological, ophthalmological, cardiovascular, digestive, musculoskeletal, renal and general toxicities and propose a timetable for examinations to be performed before and during treatment.
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http://dx.doi.org/10.1016/j.bulcan.2020.12.014DOI Listing
May 2021

Review of the Current Literature and Our Experience on the Value of OCT-angiography in White Dot Syndromes.

Ocul Immunol Inflamm 2021 Feb 22:1-15. Epub 2021 Feb 22.

DHU Sight Restore, Centre Hospitalier National Des Quinze-Vingts, Paris, France.

Purpose: To describe the application of OCT-A in various posterior uveitis disorders in our experience and to compare it with the available literature.

Methods: Eighteen eyes with the diagnoses of multifocal choroiditis (MFC), multifocal placoid pigment epitheliopathy (APMPPE), multiple evanescent white dot syndrome (MEWDS), tuberculous serpiginous-like choroiditis (SLC), serpiginous choroiditis (SC), and birdshot chorioretinopathy (BSCR) were studied.

Results: We found flow void of the choriocapillaris in patients with APMPPE, SC, MFC, BSCR, and in SLC. In contrast, perfusion of the choriocapillaris seemed normal in patients with MEWDS.

Conclusions: We confirmed that OCT-A contributes new information on the physiopathology of white dot syndromes and inflammatory chorioretinopathies, notably on whether or not the choriocapillaris is involved. Comparing the OCT-A features allowed us to suggest that both APMPPE and SLC might be part of the same spectrum of inflammatory disease with primary involvement at the level of the choriocapillaris and secondary RPE damage.
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http://dx.doi.org/10.1080/09273948.2020.1837185DOI Listing
February 2021

Optical Incoherence Tomography: a method to generate tomographic retinal cross-sections with non-interferometric adaptive optics ophthalmoscopes.

Biomed Opt Express 2020 Aug 6;11(8):4069-4084. Epub 2020 Jul 6.

DOTA, ONERA, Université Paris Saclay F-91123 Palaiseau, France.

We present Optical Incoherence Tomography (OIT): a completely digital method to generate tomographic retinal cross-sections from through-focus image stacks acquired by non-interferometric imaging systems, such as adaptive optics (AO)-ophthalmoscopes. We demonstrate that OIT can be applied to different imaging modalities using back-scattered light, including systems without inherent optical sectioning and, for the first time, multiply-scattered light, revealing a distinctive cross-sectional view of the retina. The axial dimension of OIT cross-sections is given in terms of focus position rather than optical path, as in OCT. We explore this property to guide focus position in cases where the user is "blind" focusing, allowing precise plane selection for imaging of retinal pigment epithelium, the vascular plexuses and translucent retinal neurons, such as photoreceptor inner segments and retinal ganglion cells, using respectively autofluorescence, motion contrast and split detection techniques.
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http://dx.doi.org/10.1364/BOE.396937DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7449754PMC
August 2020

Retinal Arteriolar Occlusions and Exudative Retinal Detachments in Malignant Hypertension: More Than Meets the Eye.

Am J Hypertens 2021 02;34(1):30-33

Urgences Néphrologiques et Transplantation Rénale, Hôpital Tenon, Assistance Publique Hôpitaux de Paris, Sorbonne Université, Paris, France.

Background: Malignant hypertension is macrovascular and microvascular endothelial injury responsible for multiple organ damage. Considering the anatomical and functional homologies between the posterior pole of the eye and the kidney, ophthalmological explorations may inform clinicians on the mechanisms underpinning concurrent kidney injury in this condition. More specifically, we investigated whether the wall-to-lumen ratio (WLR) of retinal arterioles measured by adaptive optics ophthalmoscopy could be correlated to WLR of kidney arterioles as determined by pathology. We sought to estimate the incidence of retinal arteriole occlusion a supposedly uncommon complication of malignant hypertension.

Methods: All patients hospitalized in our renal Intensive Care Unit for malignant hypertension between 2016 and 2019 were referred to ophthalmological examinations.

Results: Twenty-seven patients were included. Median retinal WLR was 0.39 [0.31-0.47] and was correlated with initial systolic (r = 0.56, P = 0.003) and mean blood pressure (r = 0.46, P = 0.02) upon admission. The retinal WLR was not correlated to renal pathological findings, as assessed by juxtaglomerular WLR (r = 0.38, P = 0.2), ratio of glomerulosclerosis (r = -0.39, P = 0.2), or tubulointerstitial fibrosis (r = -0.45, P = 0.08). Retinal WLR was not associated with neurological or cardiovascular end-organ damage. Branch retinal artery occlusion was detected in 18.5% of patients and exudative retinal detachment (ERD) in 29.6% of patients, without any significant correlation with canonical signs of retinal hypertension including optic disc swelling.

Conclusions: In the setting of malignant hypertension, we failed to demonstrate a significant relationship between WLR and other meaningful end-organ injuries. However, branch retinal artery occlusion and ERD may have been hitherto underestimated.
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http://dx.doi.org/10.1093/ajh/hpaa138DOI Listing
February 2021

The 10q26 Risk Haplotype of Age-Related Macular Degeneration Aggravates Subretinal Inflammation by Impairing Monocyte Elimination.

Immunity 2020 08;53(2):429-441.e8

Sorbonne Université, INSERM, CNRS, Institut de la Vision, 17 rue Moreau, F-75012 Paris, France. Electronic address:

A minor haplotype of the 10q26 locus conveys the strongest genetic risk for age-related macular degeneration (AMD). Here, we examined the mechanisms underlying this susceptibility. We found that monocytes from homozygous carriers of the 10q26 AMD-risk haplotype expressed high amounts of the serine peptidase HTRA1, and HTRA1 located to mononuclear phagocytes (MPs) in eyes of non-carriers with AMD. HTRA1 induced the persistence of monocytes in the subretinal space and exacerbated pathogenic inflammation by hydrolyzing thrombospondin 1 (TSP1), which separated the two CD47-binding sites within TSP1 that are necessary for efficient CD47 activation. This HTRA1-induced inhibition of CD47 signaling induced the expression of pro-inflammatory osteopontin (OPN). OPN expression increased in early monocyte-derived macrophages in 10q26 risk carriers. In models of subretinal inflammation and AMD, OPN deletion or pharmacological inhibition reversed HTRA1-induced pathogenic MP persistence. Our findings argue for the therapeutic potential of CD47 agonists and OPN inhibitors for the treatment of AMD.
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http://dx.doi.org/10.1016/j.immuni.2020.07.021DOI Listing
August 2020

Reverse contrast laser Doppler holography for lower frame rate retinal and choroidal blood flow imaging.

Opt Lett 2020 Jul;45(14):4012-4015

Laser Doppler holography (LDH) is an interferometric blood flow imaging technique based on full-field measurements of the Doppler spectrum. LDH has so far been demonstrated in the retina with ultrafast cameras, typically at 75 kHz. We show here that a similar method can be implemented with camera frame rates 10 times slower than before. Due to energy conservation, low and high frequency local power Doppler signals have opposite variations, and a simple contrast inversion of the low frequency power Doppler reveals fast blood flow beyond the camera detection bandwidth for conventional laser Doppler measurements. Relevant blood flow variations and color composite power Doppler images can be obtained with camera frame rates down to a few kHz.
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http://dx.doi.org/10.1364/OL.393712DOI Listing
July 2020

Spatio-temporal filtering in laser Doppler holography for retinal blood flow imaging.

Biomed Opt Express 2020 Jun 26;11(6):3274-3287. Epub 2020 May 26.

Institut Langevin. Centre National de la Recherche Scientifique (CNRS). Paris Sciences & Lettres (PSL University). École Supérieure de Physique et de Chimie Industrielles (ESPCI Paris) - 1 rue Jussieu. 75005 Paris, France.

Laser Doppler holography (LDH) is a full-field interferometric imaging technique recently applied in ophthalmology to measure blood flow, a parameter of high clinical interest. From the temporal fluctuations of digital holograms acquired at ultrafast frame rates, LDH reveals retinal and choroidal blood flow with a few milliseconds of temporal resolution. However, LDH experiences difficulties to detect slower blood flow as it requires to work with low Doppler frequency shifts which are corrupted by eye motion. We here demonstrate the use of a spatio-temporal decomposition adapted from Doppler ultrasound that provides a basis appropriate to the discrimination of blood flow from eye motion. A singular value decomposition (SVD) can be used as a simple, robust, and efficient way to separate the Doppler fluctuations of blood flow from those of strong spatial coherence such as eye motion. We show that the SVD outperforms the conventional Fourier based filter to reveal slower blood flow, and dramatically improves the ability of LDH to reveal vessels of smaller size or with a pathologically reduced blood flow.
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http://dx.doi.org/10.1364/BOE.392699DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7316027PMC
June 2020

Analyzing Age-Related Macular Degeneration Progression in Patients with Geographic Atrophy Using Joint Autoencoders for Unsupervised Change Detection.

J Imaging 2020 Jun 29;6(7). Epub 2020 Jun 29.

Clinical Imaging Center 1423, Quinze-Vingts Hospital, INSERM-DGOS Clinical Investigation Center, 75012 Paris, France.

Age-Related Macular Degeneration (ARMD) is a progressive eye disease that slowly causes patients to go blind. For several years now, it has been an important research field to try to understand how the disease progresses and find effective medical treatments. Researchers have been mostly interested in studying the evolution of the lesions using different techniques ranging from manual annotation to mathematical models of the disease. However, artificial intelligence for ARMD image analysis has become one of the main research focuses to study the progression of the disease, as accurate manual annotation of its evolution has proved difficult using traditional methods even for experienced practicians. In this paper, we propose a deep learning architecture that can detect changes in the eye fundus images and assess the progression of the disease. Our method is based on joint autoencoders and is fully unsupervised. Our algorithm has been applied to pairs of images from different eye fundus images time series of 24 ARMD patients. Our method has been shown to be quite effective when compared with other methods from the literature, including non-neural network based algorithms that still are the current standard to follow the disease progression and change detection methods from other fields.
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http://dx.doi.org/10.3390/jimaging6070057DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8321155PMC
June 2020

Non-invasive evaluation of retinal vascular remodeling and hypertrophy in humans: intricate effect of ageing, blood pressure and glycaemia.

Clin Res Cardiol 2021 Jul 3;110(7):959-970. Epub 2020 Jun 3.

Cardiovascular Prevention Unit, Department of Endocrinology and Metabolism, APHP.6 Sorbonne University, Paris, France.

Background: Ageing, hypertension and diabetes have an intricate effect on microvascular structure. In the retina, the respective contribution of remodeling and hypertrophy in such process is still unclear. We aimed at disentangling age, blood pressure and glycaemia effects on retinal microcirculation using the non-invasive adaptive optics ophthalmoscopy (AOO).

Methods: We included 429 subjects, distributed into 4 groups according to normal (nBP) or high blood pressure (hBP) and/or normal (nGly) or high fasting glycaemia (hGly). The nBP/nGly group was stratified in age tertiles to isolate the effect of ageing. AOO was used to measure arteriolar wall thickness (WT, µm), arteriolar (aID, µm) and venular internal diameter (vID, µm) and calculate arteriolar wall-to-lumen ratio (WLR), wall cross-sectional area (WCSA, µm). One-way ANOVA for parametric variables and Kruskal-Wallis test for non-parametric variables were used for comparison among groups. A multivariate regression analysis including age, gender, BP, hGly and antihypertensive treatment was performed to calculate independent predictors of retinal remodeling.

Results: WT was increased with ageing (tertile1: 22.5 ± 3.2, tertile2: 24.2 ± 3.5, tertile 3: 25.2 ± 3.8, p = 0.001) and BP (hBP: 25.2 ± 4.1 vs nBP: 23.9 ± 3.7, p = 0.003). aID decreased with BP (hBP: 90.2 ± 13.4 vs nBP: 93.6 ± 11.6, p = 0.013) and increased with glycaemia (hGly: 97.7 ± 12.5 vs nGly: 93.6 ± 11.6, p = 0.002). A multivariate analysis showed independent association of hBP with WLR; hGly with WCSA; ageing with WLR and WCSA.

Conclusions: AOO non-invasively identifies retinal structural changes in human confirming that microvascular remodeling is exclusively related to hypertension, whereas vascular growth is related to ageing and hyperglycaemia.
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http://dx.doi.org/10.1007/s00392-020-01680-3DOI Listing
July 2021

Antagonist of nucleolin, N6L, inhibits neovascularization in mouse models of retinopathies.

FASEB J 2020 04 5;34(4):5851-5862. Epub 2020 Mar 5.

CRRET Laboratory, CNRS ERL 9215, University of Paris-Est Créteil, Créteil, France.

Retinal vascular diseases (RVD) have been identified as a major cause of blindness worldwide. These pathologies, including the wet form of age-related macular degeneration, retinopathy of prematurity, and diabetic retinopathy are currently treated by intravitreal delivery of anti-vascular endothelial growth factor (VEGF) agents. However, repeated intravitreal injections can lead to ocular complications and resistance to these treatments. Thus, there is a need to find new targeted therapies. Nucleolin regulates the endothelial cell (EC) activation and angiogenesis. In previous studies, we designed a pseudopeptide, N6L, that binds the nucleolin and blocks the tumor angiogenesis. In this study, the effect of N6L was investigated in two experimental models of retinopathies including oxygen-induced retinopathy (OIR) and choroidal neovascularization (CNV). We found that in mouse OIR, intraperitoneal injection of N6L is delivered to activated ECs and induced a 50% reduction of pathological neovascularization. The anti-angiogenic effect of N6L has been tested in CNV model in which the systemic injection of N6L induced a 33% reduction of angiogenesis. This effect is comparable to those obtained with VEGF-trap, a standard of care drug for RVD. Interestingly, with preventive and curative treatments, neoangiogenesis is inhibited by 59%. Our results have potential interest in the development of new therapies targeting other molecules than VEGF for RVD.
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http://dx.doi.org/10.1096/fj.201901876RDOI Listing
April 2020

IGF-1 is an independent predictor of retinal arterioles remodeling in subjects with uncontrolled acromegaly.

Eur J Endocrinol 2020 Mar;182(3):375-383

Department of Endocrinology, Metabolism and Cardiovascular Prevention, University Hospital Pitié-Salpêtrière, APHP, Sorbonne University Paris, Paris, France.

Context: Cardiovascular disease is one of the main causes of morbidity in active acromegaly due to the increased prevalence of risk factors and arterial consequences of increased growth hormone levels. No in vivo study has evaluated the consequences of acromegaly on the retinal microvasculature.

Objective: The aim of this study was to identify in vivo the presence of morphological alterations of retinal arterioles in subjects with acromegaly.

Patients And Methods: Single-center retrospective study of a cohort of 60 subjects with acromegaly, matched to 60 controls, who were referred for adaptive optics camera (AOC) from September 2014 to December 2016. Of the subjects with acromegaly, 19 had an active disease (AD) and 41 a controlled disease (CD) based on the IGF1 ratio (IGF1r). Retinal arteriolar remodeling was previously assessed using adaptive optics camera (AOC) in order to measure wall-to-lumen ratio (WLR), wall thickness (WT), internal diameter (ID) and wall cross sectional area (WCSA).

Results: WLR was significantly higher in AD subjects compared to CD subjects and controls (AD: 0.311 ± 0.06, CD: 0.279 ± 0.04, controls: 0.281 ± 0.04, P = 0.031). A significant positive correlation was observed between WLR and IGF-1r (R2 = 0.215, P < 0.001), even after adjustment for gender, age, systolic blood pressure (SBP) and the presence of dopamine agonist treatment (R2 = 0.406, P < 0.001). Retinal arteriolar anatomical indices were comparable between CD and controls.

Conclusion: Active acromegaly is associated with the presence of small retinal arteriolar remodeling. These results provide new perspectives to better stratify cardiovascular risk and consequently optimize treatment in acromegaly.
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http://dx.doi.org/10.1530/EJE-19-0390DOI Listing
March 2020

ATTENUATION OUTER RETINAL BANDS ON OPTICAL COHERENCE TOMOGRAPHY FOLLOWING MACULAR EDEMA: A Possible Manifestation of Photoreceptor Misalignment.

Retina 2020 Nov;40(11):2232-2239

Department of Ophthalmology, PARIS Group, Quinze-Vingts Hospital, INSERM-DGOS Clinical Investigation Center, Paris, France.

Purpose: Macular edema is a common retinal disease which may leave important anatomical and functional sequelaes. Directional fundus imaging consists of comparing on- and off-axis images to reveal angle-dependent reflectance properties of fundus structures, which may be related to misaligned photoreceptors. Here, we analyzed directional optical coherence tomography (OCT) and flood-illumination adaptive optics ophthalmoscopy images to detect evidence of misaligned photoreceptors following macular edema.

Methods: Transversal, observational study. Nine patients having recovered a normal macular profile after macular edema due to retinal vein occlusion were included. For each patient, a reference OCT scan (i.e., with the incident beam normal to the fovea) was acquired, and off-axis scans were then acquired by laterally shifting the entry pupil. In addition, in four of these eyes, directional adaptive optics ophthalmoscopy documented the directional variations of cone metrics.

Results: Included patients comprised two women and seven men (age range, 19-76 years). Reference OCT scans showed patchy attenuation of the cone outer segment tips and to a lesser extent of the inner segment/outer segment lines in all, but two eyes; these. Increased intensity of the cone outer segment tips and inner segment/outer segment lines could be observed on off-axis scans. Accordingly, fusion images showed 66% average reduction of the length of cone outer segment tips attenuation. In two cases, although reference scans showed continuity of outer bands, focal attenuation was evidenced in off-axis images. Directional adaptive optics ophthalmoscopy imaging showed a strong directional variability of cone counts in these areas, ranging from near absence to roughly two-third of reference values. In each case, directional variations of cone counts paralleled those of the reflectance of outer bands.

Conclusion: After macular edema, focal attenuations of the inner segment/outer segment and of the cone outer segment tips lines may be present on OCT. These areas may show a strong directional variability by both OCT and adaptive optics ophthalmoscopy, suggesting that misaligned photoreceptor outer segments contribute to such features. The evaluation of outer retinal damage following macular edema should therefore take into account the optical Stiles-Crawford effect to disambiguate missing from misaligned cones.
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http://dx.doi.org/10.1097/IAE.0000000000002738DOI Listing
November 2020

Jointly super-resolved and optically sectioned Bayesian reconstruction method for structured illumination microscopy.

Opt Express 2019 Nov;27(23):33251-33267

Structured Illumination Microscopy (SIM) is an imaging technique for achieving both super-resolution (SR) and optical sectioning (OS) in wide-field microscopy. It consists in illuminating the sample with periodic patterns at different orientations and positions. The resulting images are then processed to reconstruct the observed object with SR and/or OS. In this work, we present BOSSA-SIM, a general-purpose SIM reconstruction method, applicable to moving objects such as encountered in in vivo retinal imaging, that enables SR and OS jointly in a fully unsupervised Bayesian framework. By modeling a 2-layer object composed of an in-focus layer and a defocused layer, we show that BOSSA-SIM is able to jointly reconstruct them so as to get a super-resolved and optically sectioned in-focus layer. The achieved performance, assessed quantitatively by simulations for several noise levels, compares favorably with a state-of-the-art method. Finally, we validate our method on open-access experimental microscopy data.
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http://dx.doi.org/10.1364/OE.27.033251DOI Listing
November 2019

Ocular injuries caused by less-lethal weapons in France.

Lancet 2019 11;394(10209):1616-1617

Department of Ophthalmology, Sorbonne Université, Pitié-Salpêtrière Hospital, Assistance Publique-Hôpitaux de Paris (AP-HP), Paris 75013, France. Electronic address:

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http://dx.doi.org/10.1016/S0140-6736(19)31807-0DOI Listing
November 2019

Waveform analysis of human retinal and choroidal blood flow with laser Doppler holography.

Biomed Opt Express 2019 Oct 5;10(10):4942-4963. Epub 2019 Sep 5.

Institut Langevin, Centre National de la Recherche Scientifique (CNRS), Paris Sciences & Lettres (PSL University), École Supérieure de Physique et de Chimie Industrielles (ESPCI Paris) - 1 rue Jussieu, 75005 Paris, France.

Laser Doppler holography was introduced as a full-field imaging technique to measure blood flow in the retina and choroid with an as yet unrivaled temporal resolution. We here investigate separating the different contributions to the power Doppler signal in order to isolate the flow waveforms of vessels in the posterior pole of the human eye. Distinct flow behaviors are found in retinal arteries and veins with seemingly interrelated waveforms. We demonstrate a full field mapping of the local resistivity index, and the possibility to perform unambiguous identification of retinal arteries and veins on the basis of their systolodiastolic variations. Finally we investigate the arterial flow waveforms in the retina and choroid and find synchronous and similar waveforms, although with a lower pulsatility in choroidal arteries. This work demonstrates the potential held by laser Doppler holography to study ocular hemodynamics in healthy and diseased eyes.
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http://dx.doi.org/10.1364/BOE.10.004942DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6788604PMC
October 2019

High-Resolution Imaging of Retinal Vasculitis by Flood Illumination Adaptive Optics Ophthalmoscopy: A Follow-up Study.

Ocul Immunol Inflamm 2020 Nov 1;28(8):1171-1180. Epub 2019 Oct 1.

Ophthalmology Department, Quinze-Vingts Hospital, INSERM-DHOS CIC 1423 , Paris, France.

: To monitor perivascular sheathing during the course of retinal vasculitis by flood illumination adaptive optics ophthalmoscopy (AOO). : Perivenous sheathing and venous diameters were quantitatively analyzed by semi-automatic segmentation of AOO images in 12 eyes of treatment-naive patients with retinal vasculitis. : The width of venous sheathing ranged from 45 to 225 µm (mean 101.0 µm ± 54.3). In 10 cases, the underlying vein showed focal narrowing (mean ± SD 14% ± 10). Focal narrowing of arteries was also present in one eye. At presentation, width of sheathing and vessel diameters were not correlated with fluorescein leakage. During follow-up, 5 eyes showed an increase in vein diameter or resolution of narrowing and in 10 eyes a thinning of vascular sheathing was observed (= .003). : Perivenous sheathing may be quantitatively analyzed and monitored by AOO. AOO may therefore contribute to monitor vascular sheathing during posterior uveitis.
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http://dx.doi.org/10.1080/09273948.2019.1646773DOI Listing
November 2020

IN VIVO OBSERVATION OF RETINAL VASCULAR DEPOSITS USING ADAPTIVE OPTICS IMAGING IN FABRY DISEASE.

Retina 2020 Aug;40(8):1623-1629

Department of Ophthalmology, Quinze-Vingts Hospital, INSERM-DHOS CIC 1423, Paris, France.

Purpose: To report a novel finding in patients with Fabry disease, that is, the observation by adaptive optics ophthalmoscopy of intracellular lipidic deposits in retinal vessels.

Methods: Observational two-center case series. Eighteen patients with genetically proven Fabry disease underwent flood-illumination adaptive optics ophthalmoscopy imaging (rtx1; Imagine Eyes, Orsay, France) of retinal vessels.

Results: Fourteen patients (78% of all patients; 7 of the 10 women and 7 of the 8 men) showed paravascular punctuate or linear opacities in both eyes. In the least-affected patients, these were seen only in the wall of precapillary arterioles as discrete spots of 5 µm to 10 µm large, whereas in those more severely affected, capillaries and first-order vessels were also involved with diffuse opacification of the wall. These deposits sometime showed a striated pattern, suggesting colocalization with vascular smooth muscle cells.

Conclusion: Adaptive optics ophthalmoscopy of retinal vessels may be of interest for patients with Fabry disease, providing noninvasive, gradable evaluation of microvascular involvement.
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http://dx.doi.org/10.1097/IAE.0000000000002648DOI Listing
August 2020

Spectral-domain optical coherence tomography of retinal vessels in Waldenström's macroglobulinemia.

Acta Ophthalmol 2020 Mar 18;98(2):153-157. Epub 2019 Aug 18.

Health and Medical Science, University of Copenhagen, Copenhagen, Denmark.

Purpose: To image retinal blood vessels in patients with Waldenström's macroglobulinemia using optical coherence tomography (OCT).

Methods: Retrospective case series examining fundus photographs and OCT scans of 16 eyes in eight patients with Waldenström's macroglobulinemia. Analyses included intravascular OCT reflectivity profiles and vessel diameters, and their relation to total immunoglobulin M (IgM) levels.

Results: In six out of eight patients, cross-sectional OCT scans of larger retinal vessels (diameter > 100 μm) showed normal intravascular reflectivity and retrovascular shadowing. In two patients with the highest total IgM > 60 g/l, altered intravascular reflectivity, distinct anterior and posterior vessel wall reflexes, and retrovascular hyposhadowing were seen. Normalization of the OCT reflectivity in these patients occurred after reduction of total IgM to < 17 g/l and was accompanied by decreasing venous tortuosity and disappearance of retinal haemorrhages and cotton wool spots.

Conclusion: This study found that Waldenström's macroglobulinemia and total IgM > 60 g/l were associated with abnormal intravascular reflectivity and retrovascular shadowing on OCT. Awareness of these signs of hyperviscosity could potentially enable earlier detection of critical conditions in patients with Waldenström's macroglobulinemia and improve the assessment of severity and treatment effect.
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http://dx.doi.org/10.1111/aos.14211DOI Listing
March 2020

Indocyanine green angiography for identifying telangiectatic capillaries in diabetic macular oedema.

Br J Ophthalmol 2020 04 29;104(4):509-513. Epub 2019 Jul 29.

Clinical Investigation Center 1423, Centre Hospitalier National d'Ophtalmologie des Quinze-Vingts, Sorbonne University, Paris, France

Aims: During diabetic macular oedema (DME), a spectrum of capillary abnormalities is commonly observed, ranging from microaneurysms to large microvascular abnormalities. Clinical evidence suggests that targeted photocoagulation of large microvascular abnormalities may be beneficial, but their detection is not done in a routine fashion. It was reported that they are better identified by indocyanine green angiography (ICGA) than by fluorescein angiography. Here, we investigated the prevalence and ICGA and optical coherence tomography (OCT) features of retinal microvascular abnormalities in a group of patients with DME.

Methods: Observational study. The fundus photographs, ICGA and structural and angiographic OCT charts of 35 eyes from 25 consecutive patients with DME were reviewed.

Results: 22 eyes (63%) had at least one focal area of microvascular abnormalities showing prolonged indocyanine green (ICG) staining (ie, beyond 10 mins after injection). In particular, all eyes (n=9) with circinate hard exudates showed foci of late ICG staining. These areas were either isolated globular capillary ecstasies or a cluster of ill-defined capillary abnormalities. They were located at a median distance of 2708 µm from the fovea (range: 1064-4583 µm). Their diameter ranged from 153 to 307 µm. During ICGA, 91% showed increased their contrast and apparent size in late frames, whereas 79% of microaneurysms showed reduced contrast on late frames. OCT angiography was not contributive for the detection of these lesions.

Conclusion: Late ICG staining revealing large microvascular abnormalities is commonly observed during DME. Because of their specific angiographic and OCT features relative to microaneurysms, we propose to name them telangiectatic capillaries (TelCaps).
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http://dx.doi.org/10.1136/bjophthalmol-2019-314355DOI Listing
April 2020

Mo-derived perivascular macrophage recruitment protects against endothelial cell death in retinal vein occlusion.

J Neuroinflammation 2019 Jul 27;16(1):157. Epub 2019 Jul 27.

INSERM, CNRS, Institut de la Vision, 17 rue Moreau, Sorbonne Université, UPMC Univ Paris 06, F-75012, Paris, France.

Background: To decipher the role of monocyte-derived macrophages (Mφs) in vascular remodeling of the occluded vein following experimental branch retinal vein occlusion (BRVO).

Methods: The inflammation induced by laser-induced BRVO on mice retina was evaluated at different time points by RT-PCR looking at inflammatory markers mRNA level expression, Icam-1, Cd11b, F4/80, Ccl2, and Ccr2 and by quantification of Iba1-positive macrophage (Mφ) density on Iba1-stained retinal flatmount. Repeated intraperitoneal EdU injection combined with liposome clodronate-induced monocyte (Mo) depletion in wildtype mice was used to differentiate Mo-derived Mφs from resident Mφs. Liposome clodronate Mo-depleted wildtype mice and Ccr2-deficient mice were used to evaluate the role of all CCR2 and CCR2 Mo-derived Mφs on EC apoptosis in the occluded vein.

Results: cd11b, ICAM-1, F4/80, Ccl2, and Ccr2 mRNA expression were increased 1, 3, and 7 days after vein occlusion. The number of parenchymal (parMφs) and perivascular (vasMφs) macrophages was increased 3 and 7 days after BRVO. The systemic depletion of all circulating Mos decreased significantly the BRVO-induced parMφs and vasMφs macrophage accumulation, while the deletion of CCR2-inflammatory Mo only diminished the accumulation of parMφs, but not vasMφs. Finally, apoptotic ECs of the vein were more numerous in fully depleted, liposome clodronate-treated mice, than in Ccr2 mice that only lack the recruitment of CCR2 inflammatory Mos.

Conclusions: BRVO triggers the recruitment of blood-derived parMφs and vasMφs. Interestingly, vasMφs accumulation was independent of CCR2. The observation that the inhibition of the recruitment of all infiltrating Mφs increases the vein EC apoptosis, while CCR2 deficiency does not, demonstrates that CCR2 Mo-derived vasMφs protect the ECs against apoptosis in the occluded vein.
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http://dx.doi.org/10.1186/s12974-019-1547-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6660930PMC
July 2019

Weibel-Palade Bodies Orchestrate Pericytes During Angiogenesis.

Arterioscler Thromb Vasc Biol 2019 09 18;39(9):1843-1858. Epub 2019 Jul 18.

From the CRRET laboratory, CNRS ERL 9215, University of Paris-Est Créteil (UPEC), France (M.C., M.D., G.C., C.H., M.P., F.R., B.V., M.-E.G., D.V., J.C., I.C.).

Objective Weibel-Palade bodies (WPBs) are endothelial cell (EC)-specific organelles formed by vWF (von Willebrand factor) polymerization and that contain the proangiogenic factor Ang-2 (angiopoietin-2). WPB exocytosis has been shown to be implicated for vascular repair and inflammatory responses. Here, we investigate the role of WPBs during angiogenesis and vessel stabilization. Approach and Results WPB density in ECs decreased at the angiogenic front of retinal vascular network during development and neovascularization compared with stable vessels. In vitro, VEGF (vascular endothelial growth factor) induced a VEGFR-2 (vascular endothelial growth factor receptor-2)-dependent exocytosis of WPBs that contain Ang-2 and consequently the secretion of vWF and Ang-2. Blocking VEGF-dependant WPB exocytosis and Ang-2 secretion promoted pericyte migration toward ECs. Pericyte migration was inhibited by adding recombinant Ang-2 or by silencing Ang-1 (angiopoietin-1) or Tie2 (angiopoietin-1 receptor) in pericytes. Consistently, in vivo anti-VEGF treatment induced accumulation of WPBs in retinal vessels because of the inhibition of WPB exocytosis and promoted the increase of pericyte coverage of retinal vessels during angiogenesis. In tumor angiogenesis, depletion of WPBs in vWF knockout tumor-bearing mice promoted an increase of tumor angiogenesis and a decrease of pericyte coverage of tumor vessels. By another approach, normalized tumor vessels had higher WPB density. Conclusions We demonstrate that WPB exocytosis and Ang-2 secretion are regulated during angiogenesis to limit pericyte coverage of remodeling vessels by disrupting Ang-1/Tie2 autocrine signaling in pericytes.
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http://dx.doi.org/10.1161/ATVBAHA.119.313021DOI Listing
September 2019

Near infrared adaptive optics flood illumination retinal angiography.

Biomed Opt Express 2019 Jun 8;10(6):2730-2743. Epub 2019 May 8.

DOTA, ONERA, Université Paris Saclay, F-91123 Palaiseau, France.

Image-based angiography is a well-adapted technique to characterize vasculature, and has been used in retinal neurovascular studies. Because the microvasculature is of particular interest, being the site of exchange between blood and tissue, a high spatio-temporal resolution is required, implying the use of adaptive optics ophthalmoscopes with a high frame rate. Creating the opportunity for decoupled stimulation and imaging of the retina makes the use of near infrared (NIR) imaging light desirable, while the need for a large field of view and a lack of distortion implies the use of a flood illumination-based setup. However, flood-illumination NIR video sequences of erythrocytes, or red blood cells (RBC), have a limited contrast compared to scanning systems and visible light. As a result, they cannot be processed via existing image-based angiography methods. We have therefore developed a new computational method relying on a spatio-temporal filtering of the sequence to isolate blood flow from noise in low-contrast sequences. Applying this computational approach enabled us to perform angiography with an adaptive optics flood illumination ophthalmoscope (AO-FIO) using NIR light, both in bright-field and dark-field modalities. Finally, we demonstrate the capabilities of our system to differentiate blood flow velocity on a retinal capillary network in vivo.
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http://dx.doi.org/10.1364/BOE.10.002730DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6583347PMC
June 2019

near-infrared autofluorescence imaging of retinal pigment epithelial cells with 757 nm excitation.

Biomed Opt Express 2018 Dec 5;9(12):5946-5961. Epub 2018 Nov 5.

Department of Ophthalmology, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA.

We demonstrate near-infrared autofluorescence (NIRAF) imaging of retinal pigment epithelial (RPE) cells in healthy volunteers and patients using a 757 nm excitation source in adaptive optics scanning laser ophthalmoscopy (AOSLO). NIRAF excited at 757 nm and collected in an emission band from 778 to 810 nm produced a robust NIRAF signal, presumably arising from melanin, and revealed the typical hexagonal mosaic of RPE cells at most eccentricities imaged within the macula of normal eyes. Several patterns of altered NIRAF structure were seen in patients, including disruption of the NIRAF over a drusen, diffuse hyper NIRAF signal with loss of individual cell delineation in a case of non-neovascular age-related macular degeneration (AMD), and increased visibility of the RPE mosaic under an area showing loss of photoreceptors. In some participants, a superposed cone mosaic was clearly visible in the fluorescence channel at eccentricities between 2 and 6° from the fovea. This was reproducible in these participants and existed despite the use of emission filters with an optical attenuation density of 12 at the excitation wavelength, minimizing the possibility that this was due to bleed through of the excitation light. This cone signal may be a consequence of cone waveguiding on either the ingoing excitation light and/or the outgoing NIRAF emitted by fluorophores within the RPE and/or choroid and warrants further investigation. NIRAF imaging at 757 nm offers efficient signal excitation and detection, revealing structural alterations in retinal disease with good contrast and shows promise as a tool for monitoring future therapies at the level of single RPE cells.
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http://dx.doi.org/10.1364/BOE.9.005946DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6490976PMC
December 2018

Higher adaptive optics loop rate enhances axial resolution in nonconfocal ophthalmoscopes.

Opt Lett 2019 May;44(9):2208-2211

In this Letter, we propose a way to better understand the impact of dynamic ocular aberrations in the axial resolution of nonconfocal adaptive optics (AO) ophthalmoscopes via a simulation of the 3D PSF in the retina for various AO-loop rates. We then use optical incoherence tomography, a method enabling the generation of tomographic retinal cross sections in incoherent imaging systems, to evaluate the benefits of a fast AO-loop rate on axial resolution and, consequently, on AO-corrected retinal image quality. We used the PARIS AO flood-illumination ophthalmoscope for this study, where retinal images from different focal planes at an AO-loop rate of 10 and 50 Hz were acquired.
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http://dx.doi.org/10.1364/OL.44.002208DOI Listing
May 2019
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